Purkinje cell activity during classical conditioning with different conditional stimuli explains central tenet of Rescorla-Wagner model

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 45, 2015, Pages 14060-14065

  Rasmussen, Anders ^a,b   Zucca, Riccardo ^c   Johansson, Fredrik ^a   Jirenhed, Dan Anders ^a   Hesslow, Germund ^a  

^a LUND UNIVERSITY   (Sweden)

^b Lund University   (Sweden)

^c UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; CELL ACTIVITY; CEREBELLUM CORTEX; COLLICULUS; CONFERENCE PAPER; EYELID REFLEX; FERRET; FIRING RATE; MALE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; REINFORCEMENT; RESCORLA WAGNER MODEL; SPIKE WAVE; STATE DEPENDENT LEARNING; SUPERIOR COLLICULUS; ANALYSIS OF VARIANCE; BLINKING; CONDITIONED REFLEX; HUMAN; LEARNING; PHYSIOLOGY; PSYCHOLOGICAL MODEL;

ANALYSIS OF VARIANCE; ASSOCIATION LEARNING; BLINKING; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; HUMANS; MODELS, PSYCHOLOGICAL; PURKINJE CELLS; REINFORCEMENT (PSYCHOLOGY);

EID: 84946763304     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1516986112     Document Type: Article

References (48)

1. Miller RR, Barnet RC, Grahame NJ (1995) Assessment of the Rescorla-Wagner model. Psychol Bull 117(3):363-386.
2. Sutton RS, Barto AG (1981) Toward a modern theory of adaptive networks: Expectation and prediction. Psychol Rev 88(2):135-170.
3. Gallistel C (1990) The Organization of Learning (Bradford Books/MIT, Cambridge, MA).
4. Rescorla RA, Wagner AR, Black AH, Prokasy WF (1972) A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. Classical Conditioning II (Appleton-Century-Crofts, New York), pp 64-99.
5. Andersson G, Garwicz M, Hesslow G (1988) Evidence for a GABA-mediated cerebellar inhibition of the inferior olive in the cat. Exp Brain Res 72(3):450-456.
6. Sears LL, Steinmetz JE (1991) Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain Res 545(1-2): 114-122.
7. Hesslow G, Ivarsson M (1996) Inhibition of the inferior olive during conditioned responses in the decerebrate ferret. Exp Brain Res 110(1):36-46.
8. Kim JJ, Krupa DJ, Thompson RF (1998) Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. Science 279(5350):570-573.
9. Medina JF, Nores WL, Mauk MD (2002) Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 416(6878):330-333.
10. Kehoe EJ, White NE (2004) Overexpectation: Response loss during sustained stimulus compounding in the rabbit nictitating membrane preparation. Learn Mem 11(4): 476-483.
11. Bengtsson F, Jirenhed D-A, Svensson P, Hesslow G (2007) Extinction of conditioned blink responses by cerebello-olivary pathway stimulation. Neuroreport 18(14):1479-1482.
12. Rasmussen A, Jirenhed D-A, Hesslow G (2008) Simple and complex spike firing patterns in Purkinje cells during classical conditioning. Cerebellum 7(4):563-566.
13. Lepora NF, Porrill J, Yeo CH, Dean P (2010) Sensory prediction or motor control? Application of Marr-Albus type models of cerebellar function to classical conditioning. Front Comput Neurosci 4:140.
14. Rasmussen A, Jirenhed DA, Wetmore DZ, Hesslow G (2014) Changes in complex spike activity during classical conditioning. Front Neural Circuits 8:90.
15. Rasmussen A, Hesslow G (2014) Feedback control of learning by the cerebello-olivary pathway. Prog Brain Res 210:103-119.
16. Bengtsson F, Svensson P, Hesslow G (2004) Feedback control of Purkinje cell activity by the cerebello-olivary pathway. Eur J Neurosci 20(11):2999-3005.
17. McCormick DA, Thompson RF (1984) Cerebellum: Essential involvement in the classically conditioned eyelid response. Science 223(4633):296-299.
18. Yeo CH, Hesslow G (1998) Cerebellum and conditioned reflexes. Trends Cogn Sci 2(9): 322-330.
19. Longley M, Yeo CH (2014) Distribution of neural plasticity in cerebellum-dependent motor learning. Prog Brain Res 210:79-101.
20. Jirenhed D-A, Hesslow G (2015) Are Purkinje cell pauses drivers of classically conditioned blink responses? Cerebellum, 10.1007/s12311-015-0722-4.
21. Jirenhed DA, Bengtsson F, Hesslow G (2007) Acquisition, extinction, and reacquisition of a cerebellar cortical memory trace. J Neurosci 27(10):2493-2502.
22. Najac M, Raman IM (2015) Integration of Purkinje cell inhibition by cerebellar nucleoolivary neurons. J Neurosci 35(2):544-549.
23. Heiney SA, Kim J, Augustine GJ, Medina JF (2014) Precise control of movement kinematics by optogenetic inhibition of Purkinje cell activity. J Neurosci 34(6): 2321-2330.
24. Hesslow G (1994) Correspondence between climbing fibre input and motor output in eyeblink-related areas in cat cerebellar cortex. J Physiol 476(2):229-244.
25. Rescorla RA (1970) Reduction in the effectiveness of reinforcement after prior excitatory conditioning. Learn Motiv (1):372-381.
26. McNally GP, Pigg M, Weidemann G (2004) Blocking, unblocking, and overexpectation of fear: A role for opioid receptors in the regulation of Pavlovian association formation. Behav Neurosci 118(1):111-120.
27. Lattal LM, Nakajima S (1998) Overexpectation in appetitive Pavlovian and instrumental conditioning. Anim Learn Behav 26(3):351-360.
28. Khallad Y, Moore J (1996) Blocking, unblocking, and overexpectation in autoshaping with pigeons. J Exp Anal Behav 65(3):575-591.
29. Bengtsson F, Hesslow G (2006) Cerebellar control of the inferior olive. Cerebellum 5(1):7-14.
30. Kehoe EJ, Macrae M (2002) Fundamental behavioral methods and findings in classical conditioning. A Neuroscientist's Guide to Classical Conditioning, ed Moore JW (Springer, New York), pp 171-231.
31. Carrel AJ, Zbarska S, Zenitsky GD, Bracha V (2012) A trigeminal conditioned stimulus yields fast acquisition of cerebellum-dependent conditioned eyeblinks. Behav Brain Res 226(1):189-196.
32. Halverson HE, Hubbard EM, Freeman JH (2009) Stimulation of the lateral geniculate, superior colliculus, or visual cortex is sufficient for eyeblink conditioning in rats. Learn Mem 16(5):300-307.
33. Steinmetz JE (1990) Classical nictitating membrane conditioning in rabbits with varying interstimulus intervals and direct activation of cerebellar mossy fibers as the CS. Behav Brain Res 38(2):97-108.
34. Rasmussen A, et al. (2013) Number of spikes in climbing fibers determines the direction of cerebellar learning. J Neurosci 33(33):13436-13440.
35. Johansson F, Jirenhed D-A, Rasmussen A, Zucca R, Hesslow G (2014) Memory trace and timing mechanism localized to cerebellar Purkinje cells. Proc Natl Acad Sci USA 111(41):14930-14934.
36. Halverson HE, Khilkevich A, Mauk MD (2015) Relating cerebellar Purkinje cell activity to the timing and amplitude of conditioned eyelid responses. J Neurosci 35(20):7813-7832.
37. Perciavalle V, et al. (2013) Consensus paper: Current views on the role of cerebellar interpositus nucleus in movement control and emotion. Cerebellum 12(5):738-757.
38. Nelson B, Mugnaini E, Strata P (1989) Origins of GABA-ergic inputs to the inferior olive. The Olivocerebellar System in Motor Control (Springer, Berlin), pp 86-107.
39. de Zeeuw CI, Holstege JC, Calkoen F, Ruigrok TJ, Voogd J (1988) A new combination of WGA-HRP anterograde tracing and GABA immunocytochemistry applied to afferents of the cat inferior olive at the ultrastructural level. Brain Res 447(2):369-375.
40. Apps R, Lee S (2002) Central regulation of cerebellar climbing fibre input during motor learning. J Physiol 541(Pt 1):301-317.
41. Hesslow G (1986) Inhibition of inferior olivary transmission by mesencephalic stimulation in the cat. Neurosci Lett 63(1):76-80.
42. Svensson P, Bengtsson F, Hesslow G (2006) Cerebellar inhibition of inferior olivary transmission in the decerebrate ferret. Exp Brain Res 168(1-2):241-253.
43. Herreros I, Verschure PF (2013) Nucleo-olivary inhibition balances the interaction between the reactive and adaptive layers in motor control. Neural Netw 47:64-71.
44. Najafi F, Medina JF (2013) Beyond "all-or-nothing" climbing fibers: Graded representation of teaching signals in Purkinje cells. Front Neural Circuits 7:115.
45. Gilbert PF (1974) A theory of memory that explains the function and structure of the cerebellum. Brain Res 70(1):1-18.
46. Chaumont J, et al. (2013) Clusters of cerebellar Purkinje cells control their afferent climbing fiber discharge. Proc Natl Acad Sci USA 110(40):16223-16228.
47. Kamin LJ (1969) Predictability, surprise attention and conditioning. Punishment and Aversive Behavior, eds Campbell BA, Church RM (Appleton-Century-Crofts, New York), pp 279-296.
48. Hesslow G (1994) Inhibition of classically conditioned eyeblink responses by stimulation of the cerebellar cortex in the decerebrate cat. J Physiol 476(2):245-256.